Chemical Profiles of Two Pheromone Glands Are Differentially Regulated by Distinct Mating Factors in Honey Bee Queens (Apis mellifera L.)

Abstract

Pheromones mediate social interactions among individuals in a wide variety of species, from yeast to mammals. In social insects such as honey bees, pheromone communication systems can be extraordinarily complex and serve to coordinate behaviors among many individuals. One of the primary mediators of social behavior and organization in honey bee colonies is queen pheromone, which is produced by multiple glands. The types and quantities of chemicals produced differ significantly between virgin and mated queens, and recent studies have suggested that, in newly mated queens, insemination volume or quantity can affect pheromone production. Here, we examine the long-term impact of different factors involved during queen insemination on the chemical composition of the mandibular and Dufour's glands, two of the major sources of queen pheromone. Our results demonstrate that carbon dioxide (an anesthetic used in instrumental insemination), physical manipulation of genital tract (presumably mimicking the act of copulation), insemination substance (saline vs. semen), and insemination volume (1 vs. 8 µl) all have long-term effects on mandibular gland chemical profiles. In contrast, Dufour's gland chemical profiles were changed only upon insemination and were not influenced by exposure to carbon dioxide, manipulation, insemination substance or volume. These results suggest that the chemical contents of these two glands are regulated by different neuro-physiological mechanisms. Furthermore, workers responded differently to the different mandibular gland extracts in a choice assay. Although these studies must be validated in naturally mated queens of varying mating quality, our results suggest that while the chemical composition of Dufour's gland is associated with mating status, that of the mandibular glands is associated with both mating status and insemination success. Thus, the queen appears to be signaling both status and reproductive quality to the workers, which may impact worker behavior and physiology as well as social organization and productivity of the colony.

Queen-produced volatiles change dynamically during reproductive swarming and are associated with changes in honey bee (Apis mellifera) worker behavior

“…We identified two compounds (heptadecane and pentadecane) that were produced by significantly more queens at liftoff and whose quantities were also significantly higher at liftoff. While previous studies of changes in pheromone production by queens have focused on relatively stable long-term differences between virgin and mated queens (Slessor et al 1990;Gilley et al 2006) or among mated queens with different mating qualities (Huang et al 2009;Niño et al 2013), our results suggest that mated queens can alter their chemical output in response to relatively short-term changes in the state of the social collective, as workers do when they release Nasonov or alarm pheromones in response to quickly shifting conditions (Pickett et al 1980;Breed et al 2004). These results suggest that queens may play a more active role in organizing the swarming process than was previously known.…”

“…QMP consists of 9-oxo-(E )-2-decenoic acid (9-ODA), (R )-and (S )-9-hydroxy-(E )-2-decenoic acid (9-HDA), methyl p -hydroxybenzoate (HOB), and 4-hydroxy-3-methyoxyphenylethanol (HVA) (Slessor et al 1988). Approximately 20 other chemical components are found in the mandibular glands, and the proportions of these components change with reproductive state and mating quality, which has an influence on worker physiology and behavior (Richard et al 2007(Richard et al , 2011Kocher et al 2009;Niño et al 2012Niño et al , 2013Peso et al 2013).…”

Disentangling the effect of insemination and ovary development on the cuticular hydrocarbon profile in the bumblebee Bombus terrestris (Hymenoptera: Apidae)

“…Richard et al (2011) further found that differences in behavioral responses appeared to not be triggered by pronounced changes in individual chemicals but rather Bby subtle changes in the overall chemical profile^. While the Dufour's gland chemical profile is associated with the number of matings, the mandibular gland profile is associated with both the number of matings and the quality of the insemination (Niño et al 2013). Effects of insemination on the cuticular profile have not yet been shown in B. terrestris ; however, there are other effects on life history traits: insemination can have a life-shortening effect and it influences the hibernation survival rate (Baer and Schmid-Hempel 2005;Greeff and SchmidHempel 2008;Ayasse and Jarau 2014).…”

When does cheating pay? Worker reproductive parasitism in honeybees

“…While queens do not increase production of QMP as their reproductive output increases Nonacs, 1993, Strauss et al, 2008), the amount of QMP produced by queens has been shown to increase with insemination volume, allowing QMP to act as an honest signal of the queen's reproductive status (Nino et al, 2013a, Nino et al, 2013b. Workers are known to respond to this signal; they are more likely to have active ovaries in the presence of an unmated queen than when they are reared with a mated queen (Peso et al, 2013).…”